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First Record of Ategmic Ovules in Orchidaceae Offers New Insights Into Mycoheterotrophic Plants

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First Record of Ategmic Ovules in Orchidaceae Offers New Insights Into Mycoheterotrophic Plants ORIGINAL RESEARCH published: 29 November 2019 doi: 10.3389/fpls.2019.01447 First Record of Ategmic Ovules in Orchidaceae Offers New Insights Into Mycoheterotrophic Plants Mariana Ferreira Alves *, Fabio Pinheiro, Marta Pinheiro Niedzwiedzki and Juliana Lischka Sampaio Mayer * Departamento de Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas, São Paulo, Brazil The number of integuments found in angiosperm ovules is variable. In orchids, most species show bitegmic ovules, except for some mycoheterotrophic species that show ovules with only one integument. Analysis of ovules and the development of the seed coat provide important information regarding functional aspects such as dispersal and seed germination. This study aimed to analyze the origin and development of the seed coat of the mycoheterotrophic orchid Pogoniopsis schenckii and to compare this development with that of other photosynthetic species of the family. Flowers and Edited by: fruits at different stages of development were collected, and the usual methodology Jen-Tsung Chen, National University of Kaohsiung, for performing anatomical studies, scanning microscopy, and transmission microscopy Taiwan following established protocols. P. schenckii have ategmic ovules, while the other species Reviewed by: are bitegmic. No evidence of integument formation at any stage of development was David Smyth, found through anatomical studies. The reduction of integuments found in the ovules Monash University, Australia Dennis William Stevenson, could facilitate fertilization in this species. The seeds of P. schenckii, Vanilla planifolia, and New York Botanical Garden, V. palmarum have hard seed coats, while the other species have seed coats formed by United States the testa alone, making them thin and transparent. P. schenckii, in contrast to the other *Correspondence: Mariana Ferreira Alves species analyzed, has a seed coat that originates from the nucellar epidermis, while in [email protected] other species, the seed coat originates from the outer integument. Juliana Lischka Sampaio Mayer [email protected] Keywords: anatomy, integument, Epidendroideae, saprophytic, Vanilloideae Specialty section: This article was submitted to INTRODUCTION Plant Development and EvoDevo, a section of the journal Flowers are highly variable structures, resulting in a great morphological diversity and a variety of Frontiers in Plant Science adaptive processes in angiosperms (Endress, 1994; Friis et al., 2011). Variations in flower size and Received: 05 July 2019 number of whorls, besides the presence or absence of fused floral parts, are caused by differences Accepted: 17 October 2019 that occur during the development of floral organs. Plants exhibit open organization, which means Published: 29 November 2019 that their organs are generally exposed, and that they do not have any organ or parts of organs Citation: internalized, with the exception of carpels (Endress, 2015). In turn, carpels can be free or united, Alves MF, Pinheiro F, Niedzwiedzki MP becoming curved during their initial development, with edges getting closed or sealed when they and Mayer JLS (2019) First Record of are fully developed (Endress, 2006). While most floral organs are exposed, mainly due to the action Ategmic Ovules in Orchidaceae Offers New Insights Into of pollinating agents (e.g., animals, wind, and water), ovules are completely enclosed in the carpel a Mycoheterotrophic Plants. condition known as angiospermy (Endress, 2006). Front. Plant Sci. 10:1447. Ovules are female reproductive structures that develop in the seeds (Bouman, 1984; Endress, 2011). doi: 10.3389/fpls.2019.01447 Despite their relatively stable basic structure, ovules have a wide diversity of form, varying in terms of Frontiers in Plant Science | www.frontiersin.org 1 November 2019 | Volume 10 | Article 1447 Alves et al. Ategmic Ovules in Orchidaceae their position in the ovary, size, curvature, number and thickness of mycoheterotrophic species evolved several times independently integument, funiculus length, and degree of vascularization (Endress, (Li et al., 2019). In the family, 235 species with this condition 2011). For angiosperms, there are records of bitegmic, unitegmic, are described (Merckx et al., 2013), and little is known about the and ategmic species (Bouman, 1984; Endress, 2011). Although most reproductive process of these species. Owing to the importance of angiosperms are bitegmic, variation in the number and thickness the seed coat in the life cycle of plants, and because it is considered of integuments can be observed at different taxonomic levels, such a stable characteristic, understanding its structure and development as in families and genera. For example, in Olacaceae, there are can reveal information relevant to its functional aspects, such as described bitegmic, unitegmic, and ategmic species (Brown et al., dispersal and seed germination (Bouman, 1984; Windsor et al., 2000; 2010). In Melastomataceae, ovules are bitegmic; however, in species Endress, 2011). Thus, the objective of this work was to analyze the of the same genus, the number of the outer integument layers can origin and development of the seed coat of the mycoheterotrophic vary from two to many (Caetano et al., 2018). orchid Pogoniopsis schenckii Cogn, and to compare this development Previous studies have described the main function of with that of other species in the family that have chlorophyll integuments as the delimitation of the micropyle, and protection and present different mechanisms of seed dispersal, Polystachya to the embryo sac and embryo (Herrero, 2001); however, they estrellensis Rchb.f., Elleanthus brasiliensis Rchb.f., Isochilus linearis may also have other functions in species of different families. (Jacq) Barb.Rodr., and Cleistes libonii (Rchb. f.) Schltr.—species For example, the inner epidermis of the inner integument can that exhibit anemochory, and Vanilla planifolia Jacks. ex Andrews function as a secretory tissue, playing a role in the nutrition of and Vanilla palmarum (Salzm ex. Lindl.) Lindl.—species showing the embryonic sac. This layer of cells is known as integumentary evidence of zoochory (Cribb, 1999). Pogoniopsis schenckii is an tapetum (Kapil and Tiwari, 1978). Another hypothesis is that the endemic mycoheterotrophic species found in the Brazilian Atlantic number of integument layers could be related to the fruit type Forest. Prior studies indicate a tendency of reduction in the number and seed dispersal mode. A study performed with several species of integuments in species of mycoheterotrophic plants, including of Melastomataceae tried to confirm if there was a relationship orchids (Abe, 1976; Arekal and Karanth, 1981; Maas and Ruyters, between ovules with multiseriate outer integument and fleshy 1986; Bouman et al., 2002; Endress, 2011; Krawczyk et al., 2016; Li fruits (Caetano et al., 2018). The data obtained did not confirm this et al., 2016). Thus, our hypothesis is thatP. schenckii also exhibits relation; however, ancestral state reconstruction shows a tendency reduction in the number of integuments, leading to a greater for ovules with multiseriate outer integument to occur in fleshy fruit exposure of the ovule and simplification of the seed coat involving clades. Recent studies conducted with Arabidopsis show that the the embryo, which may facilitate the penetration of fungal hyphae. number of ovule integument layers is related to gene and hormone In this context, structural information on the reproductive organs of expression (Bencivenga et al., 2012; Gomez et al., 2016; Coen and mycoheterotrophic species, especially P. schenckii, can contribute to Magnani, 2018) and may be responsible for the seed coat diversity the elucidation of processes related to the symbiosis between fungi observed in angiosperms. After fertilization, the integument layers and mycoheterotrophic species. In addition, since the mode of seed go through different pathways to establish a protective barrier for dispersal of P. schenckii is not known, characterization of the stages the embryo (Windsor et al., 2000). There is an immense diversity in of development of its seeds can contribute to the understanding of seed structure, such as size, color, texture, and shape; this diversity the ecological interactions involved in the dispersal and colonization is related to dispersal and germination strategies (Boesewinkel and of new habitats. Bouman, 1984), and may have been initially determined by the arrangement and number of ovule integuments. In most angiosperms, the formation of ovules is complete MATERIAL AND METHODS when anthesis starts. In Orchidaceae, however, a different pattern is observed, where in the development of ovules and Species Studied and Literature Review their respective placental proliferation are conditioned to the Pogoniopsis schenckii Cogn. -Epidendroideae- is aclorophyllated pollination event (Swamy, 1949a). In general, orchids have and remains underground for almost its entire life cycle. During low reproductive success because of low pollination rates its reproductive phase, a floral stem appears above ground level; (Cozzolino and Widmer, 2005). Thus, ovules will be produced afterwards, flowers and fruits develop.Polystachya estrellensis only if there is guaranteed seed formation, in order to prevent Rchb. f., Elleanthus brasiliensis Rchb. f., Isochilus linearis (Jacq) unnecessary energy expenditure (Arditti, 1992). The formation Barb. Rodr., belonging to the subfamily Epidendroideae, and of
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